Key Points
-
Lewontin's paradox — the much larger variation in species abundance than in genetic diversity — is closer to being explained.
-
The reproductive strategy of species has an impact on genome-wide diversity, providing a connection between population dynamic processes and the long-term effective population size (Ne).
-
Selection at linked sites also affects genome-wide diversity, but not to an extent that it is sufficient alone to explain Lewontin's paradox.
-
Selection and demography, among other factors, contribute to variation in Ne within genomes and leads to variation in diversity in different genomic regions of the same species.
Abstract
Genetic polymorphism varies among species and within genomes, and has important implications for the evolution and conservation of species. The determinants of this variation have been poorly understood, but population genomic data from a wide range of organisms now make it possible to delineate the underlying evolutionary processes, notably how variation in the effective population size (Ne) governs genetic diversity. Comparative population genomics is on its way to providing a solution to 'Lewontin's paradox' — the discrepancy between the many orders of magnitude of variation in population size and the much narrower distribution of diversity levels. It seems that linked selection plays an important part both in the overall genetic diversity of a species and in the variation in diversity within the genome. Genetic diversity also seems to be predictable from the life history of a species.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$189.00 per year
only $15.75 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
Change history
08 June 2016
In the original version of this article, the author name in reference 73 (Stebbins, G. L. Self fertilization and population variability in the higher plants. Am. Naturalist 91, 41–46 (1957)) was mis-spelled. This has now been corrected. The authors apologise for this error.
References
Lewontin, R. C. & Hubby, J. L. A molecular approach to the study of genic heterozygosity in natural populations. II. Amount of variation and degree of heterozygosity in natural populations of Drosophila pseudoobscura. Genetics 54, 595–609 (1966).
Harris, H. Enzyme polymorphisms in man. Proc. R. Soc. Lond. B 164, 298–310 (1966).
Quintana-Murci, L. & Clark, A. G. Population genetic tools for dissecting innate immunity in humans. Nat. Rev. Immunol. 13, 280–293 (2013).
Bodmer, W. Genetic characterization of human populations: from ABO to a genetic map of the British people. Genetics 199, 267–279 (2015).
Hake, S. & Ross-Ibarra, J. Genetic, evolutionary and plant breeding insights from the domestication of maize. eLife 4, e05861 (2015).
Soares, M. P. & Weiss, G. The Iron Age of host–microbe interactions. EMBO Rep. 16, 1482–1500 (2015).
Vander Wal, E., Garant, D., Festa-Bianchet, M. & Pelletier, F. Evolutionary rescue in vertebrates: evidence, applications and uncertainty. Phil. Trans. R. Soc. B 368, 20120090 (2012).
Forcada, J. & Hoffman, J. I. Climate change selects for heterozygosity in a declining fur seal population. Nature 511, 462–465 (2014).
Begun, D. J. et al. Population genomics: whole-genome analysis of polymorphism and divergence in Drosophila simulans. PLoS Biol. 5, e310 (2007).
Lack, J. B. et al. The Drosophila genome nexus: a population genomic resource of 623 Drosophila melanogaster genomes, including 197 from a single ancestral range population. Genetics 199, 1229–1241 (2015).
McVean, G., Spencer, C. C. A. & Chaix, R. Perspectives on human genetic variation from the HapMap project. PLoS Genet. 1, e54 (2005).
The 1000 Genomes Project Consortium. A global reference for human genetic variation. Nature 526, 68–74 (2015).
Tenaillon, M. I. et al. Patterns of DNA sequence polymorphism along chromosome 1 of maize (Zea mays ssp. mays L.). Proc. Natl Acad. Sci. USA 98, 9161–9166 (2001).
Nordborg, M. et al. The pattern of polymorphism in Arabidopsis thaliana. PLoS Biol. 3, e196 (2005).
Doniger, S. W. et al. A catalog of neutral and deleterious polymorphism in yeast. PLoS Genet. 4, e1000183 (2008).
Wong, G. K. S. et al. A genetic variation map for chicken with 2.8 million single-nucleotide polymorphisms. Nature 432, 717–722 (2004).
Sachidanandam, R. et al. A map of human genome sequence variation containing 1.42 million single nucleotide polymorphisms. Nature 409, 928–933 (2001).
Hodgkinson, A. & Eyre-Walker, A. Variation in the mutation rate across mammalian genomes. Nat. Rev. Genet. 12, 756–766 (2011).
Lynch, M. Evolution of the mutation rate. Trends Genet. 26, 345–352 (2010).
Charlesworth, B. Effective population size and patterns of molecular evolution and variation. Nat. Rev. Genet. 10, 195–205 (2009).
Kimura, M. The Neutral Theory of Molecular Evolution (Cambridge Univ. Press, 1983).
Lewontin, R. The Genetic Basis of Evolutionary Change (Columbia Univ. Press, 1974). This book is a remarkably clear and early introduction to the problem of variation in genetic diversity and the first statement of the so-called Lewontin's paradox.
Leffler, E. M. et al. Revisiting an old riddle: what determines genetic diversity levels within species? PLoS Biol. 10, e1001388 (2012). This article contains a thorough review of the distribution of DNA sequence diversity across hundreds of eukaryotic species.
Reed, D. H. & Frankham, R. Correlation between fitness and genetic diversity. Conserv. Biol. 17, 230–237 (2003).
Reed, D. H. & Frankham, R. How closely correlated are molecular and quantitative measures of genetic variation? A meta-analysis. Evolution 55, 1095–1103 (2001).
Bjørnstad, O. N. & Grenfell, B. T. Noisy clockwork: time series analysis of population fluctuations in animals. Science 293, 638–643 (2001).
Sun, J., Cornelius, S. P., Janssen, J., Gray, K. A. & Motter, A. E. Regularity underlies erratic population abundances in marine ecosystems. J. R. Soc. Interface 12, 20150235 (2015).
Banks, S. C. et al. How does ecological disturbance influence genetic diversity? Trends Ecol. Evol. 28, 670–679 (2013).
Alcala, N. & Vuilleumier, S. Turnover and accumulation of genetic diversity across large time-scale cycles of isolation and connection of populations. Proc. R. Soc. B 281, 20141369 (2014).
Mayr, E. Animal Species and Evolution (Harvard Univ. Press, 1963).
Hewitt, G. The genetic legacy of the Quaternary ice ages. Nature 405, 907–913 (2000).
Stuessy, T. F., Takayama, K., López-Sepúlveda, P. & Crawford, D. J. Interpretation of patterns of genetic variation in endemic plant species of oceanic islands. Bot. J. Linnean Soc. 174, 276–288 (2014).
Aguilar, R., Quesada, M., Ashworth, L., Herrerias-Diego, Y. & Lobo, J. Genetic consequences of habitat fragmentation in plant populations: susceptible signals in plant traits and methodological approaches. Mol. Ecol. 17, 5177–5188 (2008).
Caplins, S. A. et al. Landscape structure and the genetic effects of a population collapse. Proc. R. Soc. B 281, 20141798 (2014).
Coltman, D. W. Molecular ecological approaches to studying the evolutionary impact of selective harvesting in wildlife. Mol. Ecol. 17, 221–235 (2008).
Lynch, M. The Origins of Genome Architecture (Sinauer Associates, 2007).
Romiguier, J. et al. Comparative population genomics in animals uncovers the determinants of genetic diversity. Nature 515, 261–263 (2014). This study shows a comparative analysis of patterns of diversity across animals revealing a strong influence of the life-history traits of species.
Sung, W., Ackerman, M. S., Miller, S. F., Doak, T. G. & Lynch, M. Drift-barrier hypothesis and mutation-rate evolution. Proc. Natl Acad. Sci. USA 109, 18488–18492 (2012).
Ness, R. W., Morgan, A. D., Vasanthakrishnan, R. B., Colegrave, N. & Keightley, P. D. Extensive de novo mutation rate variation between individuals and across the genome of Chlamydomonas reinhardtii. Genome Res. 25, 1739–1749 (2015).
Wright, S. Size of population and breeding structure in relation to evolution. Science 87, 430–431 (1938).
Weber, D., Stewart, B. S., Garza, J. C. & Lehman, N. An empirical genetic assessment of the severity of the northern elephant seal population bottleneck. Curr. Biol. 10, 1287–1290 (2000).
Hedrick, P. W. Conservation genetics and North American bison (Bison bison). J. Hered. 100, 411–420 (2009).
Spielman, D., Brook, B. W. & Frankham, R. Most species are not driven to extinction before genetic factors impact them. Proc. Natl Acad. Sci. USA 101, 15261–15264 (2004).
Nabholz, B., Mauffrey, J. -F., Bazin, E., Galtier, N. & Glemin, S. Determination of mitochondrial genetic diversity in mammals. Genetics 178, 351–361 (2008).
McCusker, M. R. & Bentzen, P. Positive relationships between genetic diversity and abundance in fishes. Mol. Ecol. 19, 4852–4862 (2010).
Perry, G. H. et al. Comparative RNA sequencing reveals substantial genetic variation in endangered primates. Genome Res. 22, 602–610 (2012).
Pinsky, M. L. & Palumbi, S. R. Meta-analysis reveals lower genetic diversity in overfished populations. Mol. Ecol. 23, 29–39 (2014).
Ho, S. Y. W. & Shapiro, B. Skyline-plot methods for estimating demographic history from nucleotide sequences. Mol. Ecol. Resour. 11, 423–434 (2011).
Drummond, A. J., Rambaut, A., Shapiro, B. & Pybus, O. G. Bayesian coalescent inference of past population dynamics from molecular sequences. Mol. Biol. Evol. 22, 1185–1192 (2005).
Li, H. & Durbin, R. Inference of human population history from individual whole-genome sequences. Nature 475, 493–496 (2011).
Liu, X. & Fu, Y. -X. Exploring population size changes using SNP frequency spectra. Nat. Genet. 47, 555–559 (2015).
Schiffels, S. & Durbin, R. Inferring human population size and separation history from multiple genome sequences. Nat. Genet. 46, 919–925 (2014).
Nadachowska-Brzyska, K., Li, C., Smeds, L., Zhang, G. & Ellegren, H. Temporal dynamics of avian populations during Pleistocene revealed by whole-genome sequences. Curr. Biol. 25, 1375–1380 (2015).
Jarne, P. Mating system, bottlenecks and genetic polymorphism in hermaphroditic animals. Genet. Res. 65, 193–207 (1995).
Charlesworth, D. & Wright, S. Breeding systems and genome evolution. Curr. Opin. Genet. Dev. 11, 685–690 (2001).
Glémin, S., Bazin, E. & Charlesworth, D. Impact of mating systems on patterns of sequence polymorphism in flowering plants. Proc. R. Soc. B 273, 3011–3019 (2006).
Glémin, S. & Muyle, A. Mating systems and selection efficacy: a test using chloroplastic sequence data in angiosperms. J. Evol. Biol. 27, 1386–1399 (2014).
Hartfield, M. Evolutionary genetic consequences of facultative sex and outcrossing. J. Evol. Biol. 29, 5–22 (2016). This review discusses the theoretical predictions and empirical evidence regarding genome evolution in asexual versus sexual contexts.
Slotte, T. et al. The Capsella rubella genome and the genomic consequences of rapid mating system evolution. Nat. Genet. 45, 831–835 (2013).
Burgarella, C. et al. Molecular evolution of freshwater snails with contrasting mating systems. Mol. Biol. Evol. 32, 2403–2416 (2015).
Thomas, C. G. et al. Full-genome evolutionary histories of selfing, splitting, and selection in Caenorhabditis. Genome Res. 25, 667–678 (2015).
Dey, A., Chan, C. K. W., Thomas, C. G. & Cutter, A. D. Molecular hyperdiversity defines populations of the nematode Caenorhabditis brenneri. Proc. Natl Acad. Sci. USA 110, 11056–11060 (2013).
Dolgin, E. S., Charlesworth, B. & Cutter, A. D. Population frequencies of transposable elements in selfing and outcrossing Caenorhabditis nematodes. Genet. Res. 90, 317–329 (2008).
Wright, S. I., Kalisz, S. & Slotte, T. Evolutionary consequences of self-fertilization in plants. Proc. R. Soc. B 280, 20130133 (2013).
Balloux, F., Lehmann, L. & de MeeÛs, T. The population genetics of clonal and partially clonal diploids. Genetics 164, 1635–1644 (2003).
Mark Welch, D. B. & Meselson, M. Evidence for the evolution of Bdelloid rotifers without sexual reproduction or genetic exchange. Science 288, 1211–1215 (2000).
Delmotte, F. et al. Phylogenetic evidence for hybrid origins of asexual lineages in an aphid species. Evolution 57, 1291–1303 (2003).
Schaefer, I. et al. No evidence for the 'Meselson effect' in parthenogenetic oribatid mites (Oribatida, Acari). J. Evol. Biol. 19, 184–193 (2006).
Schwander, T., Henry, L. & Crespi Bernard, J. Molecular evidence for ancient asexuality in Timema stick insects. Curr. Biol. 21, 1129–1134 (2011).
Hollister, J. D. et al. Recurrent loss of sex is associated with accumulation of deleterious mutations in Oenothera. Mol. Biol. Evol. 32, 896–905 (2015).
Maynard Smith, J. The Evolution of Sex (Cambridge Univ. Press, 1978).
McDonald, M. J., Rice, D. P. & Desai, M. M. Sex speeds adaptation by altering the dynamics of molecular evolution. Nature 531, 233–236 (2016).
Stebbins, G. L. Self fertilization and population variability in the higher plants. Am. Naturalist 91, 41–46 (1957).
Judson, O. P. & Normark, B. B. Ancient asexual scandals. Trends Ecol. Evol. 11, 41–46 (1996).
Simon, J. C., Delmotte, F., Rispe, C. & Crease, T. Phylogenetic evidence for hybrid origins of asexual lineages in an aphid species. Evolution 57, 1291–1303 (2003).
Igic, B. & Busch, J. W. Is self-fertilization an evolutionary dead end? New Phytol. 198, 386–397 (2013).
Tajima, F. Relationship between DNA polymorphism and fixation time. Genetics 125, 447–454 (1990).
Cutter, A. D. & Payseur, B. A. Genomic signatures of selection at linked sites: unifying the disparity among species. Nat. Rev. Genet. 14, 262–274 (2013).
Maynard Smith, J. & Haigh, J. The hitch-hiking effect of a favourable gene. Genet. Res. 23, 23–35 (1974).
Kaplan, N. L., Hudson, R. R. & Langley, C. H. The “hitchhiking effect” revisited. Genetics 123, 887–899 (1989).
Gillespie, J. H. Genetic drift in an infinite population: the pseudohitchhiking model. Genetics 155, 909–919 (2000).
Gillespie, J. H. Is the population size of a species relevant to its evolution? Evolution 55, 2161–2169 (2001). This paper shows a theoretical examination of the effects of recurrent adaptive substitutions on linked loci and their relationship to N e.
Charlesworth, B., Morgan, M. T. & Charlesworth, D. The effect of deleterious mutations on neutral molecular variation. Genetics 134, 1289–1303 (1993). This study shows a theoretical examination of the effects of recurrent deleterious substitutions on linked loci and the background selection model.
Charlesworth, B. The effect of background selection against deleterious mutations on weakly selected, linked variants. Genet. Res. 63, 213–227 (1994).
Corbett-Detig, R. B., Hartl, D. L. & Sackton, T. B. Natural selection constrains neutral diversity across a wide range of species. PLoS Biol. 13, e1002112 (2015). This article demonstrates the role of linked selection in shaping the within-genome variation in polymorphism and its relationship with N e.
Coop, G. Does linked selection explain the narrow range of genetic diversity across species? bioRxiv http://dx.doi.org/10.1101/042598 (2016).
Elyashiv, E. et al. A genomic map of the effects of linked selection in Drosophila. arXiv http://arXiv.org//abs/1408.5461v1 (2014).
Comeron, J. M. Background selection as baseline for nucleotide variation across the Drosophila genome. PLoS Genet. 10, e1004434 (2014).
Enard, D., Messer, P. W. & Petrov, D. A. Genome-wide signals of positive selection in human evolution. Genome Res. 24, 885–895 (2014).
Gossmann, T. I., Woolfit, M. & Eyre-Walker, A. Quantifying the variation in the effective population size within a genome. Genetics 189, 1389–1402 (2011).
Wu, C.-I. The genic view of the process of speciation. J. Evol. Biol. 14, 851–865 (2001).
Begun, D. J. & Aquadro, C. F. Levels of naturally occurring DNA polymorphism correlate with recombination rates in D. melanogaster. Nature 356, 519–520 (1992).
Nachman, M. W. Single nucleotide polymorphisms and recombination rate in humans. Trends Genet. 17, 481–485 (2001).
Lercher, M. J. & Hurst, L. D. Human SNP variability and mutation rate are higher in regions of high recombination. Trends Genet. 18, 337–340 (2002).
Dvorak, J., Luo, M. C. & Yang, Z. L. Restriction fragment length polymorphism and divergence in the genomic regions of high and low recombination in self-fertilizing and cross-fertilizing Aegilops species. Genetics 148, 423–434 (1998).
Stephan, W. & Langley, C. H. DNA polymorphism in Lycopersicon and crossing-over per physical length. Genetics 150, 1585–1593 (1998).
Cutter, A. D. & Choi, J. Y. Natural selection shapes nucleotide polymorphism across the genome of the nematode Caenorhabditis briggsae. Genome Res. 20, 1103–1111 (2010).
Fay, J. C. & Wu, C. I. Hitchhiking under positive Darwinian selection. Genetics 155, 1405–1413 (2000).
Campos, J. L., Halligan, D. L., Haddrill, P. R. & Charlesworth, B. The relation between recombination rate and patterns of molecular evolution and variation in Drosophila melanogaster. Mol. Biol. Evol. 31, 1010–1028 (2014).
Messer, P. W. & Petrov, D. A. Frequent adaptation and the McDonald–Kreitman test. Proc. Natl Acad. Sci. USA 110, 8615–8620 (2013).
Sella, G., Petrov, D. A., Przeworski, M. & Andolfatto, P. Pervasive natural selection in the Drosophila genome? PLoS Genet. 5, e1000495 (2009). This article reviews the evidence for a pervasive role of linked selection on patterns of genetic variation in Drosophila species.
Slotte, T. The impact of linked selection on plant genomic variation. Brief. Funct. Genomics 13, 268–275 (2014).
Lohmueller, K. E. et al. Natural selection affects multiple aspects of genetic variation at putatively neutral sites across the human genome. PLoS Genet. 7, e1002326 (2011).
Messer, P. W. SLiM: simulating evolution with selection and linkage. Genetics 194, 1037–1039 (2013).
Hernandez, R. D. A flexible forward simulator for populations subject to selection and demography. Bioinformatics 24, 2786–2787 (2008).
Bank, C., Ewing, G. B., Ferrer-Admettla, A., Foll, M. & Jensen, J. D. Thinking too positive? Revisiting current methods of population genetic selection inference. Trends Genet. 30, 540–546 (2014).
Coop, G. & Ralph, P. Patterns of neutral diversity under general models of selective sweeps. Genetics 192, 205–224 (2012).
Bolívar, P., Mugal, C. F., Nater, A. & Ellegren, H. Recombination rate variation modulates gene sequence evolution mainly via GC-biased gene conversion, not Hill–Robertson interference, in an avian system. Mol. Biol. Evol. 33, 216–227 (2016).
Payseur, B. A. & Nachman, M. W. Gene density and human nucleotide polymorphism. Mol. Biol. Evol. 19, 336–340 (2002).
Charlesworth, B. Background selection and patterns of genetic diversity in Drosophila melanogaster. Genet. Res. 68, 131–149 (1996).
Hudson, R. R. & Kaplan, N. L. Deleterious background selection with recombination. Genetics 141, 1605–1617 (1995).
Nordborg, M., Charlesworth, B. & Charlesworth, D. The effect of recombination on background selection. Genet. Res. 67, 159–174 (1996).
Flowers, J. M. et al. Natural selection in gene-dense regions shapes the genomic pattern of polymorphism in wild and domesticated rice. Mol. Biol. Evol. 29, 675–687 (2012).
Burri, R. et al. Linked selection and recombination rate variation drive the evolution of the genomic landscape of differentiation across the speciation continuum of Ficedula flycatchers. Genome Res. 25, 1656–1665 (2015). This study is a high-resolution examination of genome-wide patterns of diversity and the role of recombination and linked selection in several species of flycatcher.
Nabholz, B. et al. Transcriptome population genomics reveals severe bottleneck and domestication cost in the African rice (Oryza glaberrima). Mol. Ecol. 23, 2210–2227 (2014).
Hellmann, I., Ebersberger, I., Ptak, S. E., Pääbo, S. & Przeworski, M. A neutral explanation for the correlation of diversity with recombination rates in humans. Am. J. Hum. Genet. 72, 1527–1535 (2003).
Yang, S. et al. Parent-progeny sequencing indicates higher mutation rates in heterozygotes. Nature 523, 463–467 (2015).
Arbeithuber, B., Betancourt, A. J., Ebner, T. & Tiemann-Boege, I. Crossovers are associated with mutation and biased gene conversion at recombination hotspots. Proc. Natl Acad. Sci. USA 112, 2109–2114 (2015).
Rattray, A., Santoyo, G., Shafer, B. & Strathern, J. N. Elevated mutation rate during meiosis in Saccharomyces cerevisiae. PLoS Genet. 11, e1004910 (2015).
Duret, L. & Galtier, N. Biased gene conversion and the evolution of mammalian genomic landscapes. Annu. Rev. Genom. Hum. Genet. 10, 285–311 (2009).
Wallberg, A., Glémin, S. & Webster, M. T. Extreme recombination frequencies shape genome variation and evolution in the honeybee, Apis mellifera. PLoS Genet. 11, e1005189 (2015).
Hammer, M. F. et al. The ratio of human X chromosome to autosome diversity is positively correlated with genetic distance from genes. Nat. Genet. 42, 830–831 (2010).
Arbiza, L., Gottipati, S., Siepel, A. & Keinan, A. Contrasting X-linked and autosomal diversity across 14 human populations. Am. J. Hum. Genet. 94, 827–844 (2014).
Gottipati, S., Arbiza, L., Siepel, A., Clark, A. G. & Keinan, A. Analyses of X-linked and autosomal genetic variation in population-scale whole genome sequencing. Nat. Genet. 43, 741–743 (2011).
Charlesworth, B. The role of background selection in shaping patterns of molecular evolution and variation: evidence from variability on the Drosophila X chromosome. Genetics 191, 233–246 (2012).
Frankham, R. How closely does genetic diversity in finite populations conform to predictions of neutral theory? Large deficits in regions of low recombination. Heredity 108, 167–178 (2012). This paper reviews and demonstrates the reduction in genetic diversity in low-recombining genomic regions, including sex chromosomes, in plants and animals.
Mank, J. E., Vicoso, B., Berlin, S. & Charlesworth, B. Effective population size and the faster-X effect: empirical results and their interpretation. Evolution 64, 663–674 (2010).
Corl, A. & Ellegren, H. The genomic signature of sexual selection in the genetic diversity of the sex chromosomes and autosomes. Evolution 66, 2138–2149 (2012).
Huang, H. & Rabosky, D. L. Sex-linked genomic variation and its relationship to avian plumage dichromatism and sexual selection. BMC Evol. Biol. 15, 199 (2015).
Smeds, L. et al. Genomic identification and characterization of the pseudoautosomal region in highly differentiated avian sex chromosomes. Nat. Commun. 5, 5448 (2014).
Lien, S., Szyda, J., Schechinger, B., Rappold, G. & Arnheim, N. Evidence for heterogeneity in recombination in the human pseudoautosomal region: high resolution analysis by sperm typing and radiation-hybrid mapping. Am. J. Hum. Genet. 66, 557–566 (2000).
Bussell, J. J., Pearson, N. M., Kanda, R., Filatov, D. A. & Lahn, B. T. Human polymorphism and human–chimpanzee divergence in pseudoautosomal region correlate with local recombination rate. Gene 368, 94–100 (2006).
Charlesworth, B. & Charlesworth, D. The degeneration of Y chromosomes. Phil. Trans. R. Soc. Lond. B 355, 1563–1572 (2000).
Bachtrog, D. Y-chromosome evolution: emerging insights into processes of Y-chromosome degeneration. Nat. Rev. Genet. 14, 113–124 (2013).
Mank, J. E. Small but mighty: the evolutionary dynamics of W and Y sex chromosomes. Chromosome Res. 20, 21–33 (2011).
Hellborg, L. & Ellegren, H. Low levels of nucleotide diversity in mammalian Y chromosomes. Mol. Biol. Evol. 21, 158–163 (2004).
Bachtrog, D., Thornton, K., Clark, A., Andolfatto, P. & Harrison, R. Extensive introgression of mitochondrial DNA relative to nuclear genes in the Drosophila yakuba species group. Evolution 60, 292–302 (2006).
Shen, P. et al. Population genetic implications from sequence variation in four Y chromosome genes. Proc. Natl Acad. Sci. USA 97, 7354–7359 (2000).
Qiu, S., Bergero, R., Forrest, A., Kaiser, V. B. & Charlesworth, D. Nucleotide diversity in Silene latifolia autosomal and sex-linked genes. Proc. R. Soc. B 277, 3283–3290 (2010).
Filatov, D. A., Laporte, V., Vitte, C. & Charlesworth, D. DNA diversity in sex-linked and autosomal genes of the plant species Silene latifolia and Silene dioica. Mol. Biol. Evol. 18, 1442–1454 (2001).
Smeds, L. et al. Evolutionary analysis of the female-specific avian W chromosome. Nat. Commun. 6, 7330 (2015).
Wilson Sayres, M. A., Lohmueller, K. E. & Nielsen, R. Natural selection reduced diversity on human Y chromosomes. PLoS Genet. 10, e1004064 (2014).
Ellegren, H. Characteristics, causes and evolutionary consequences of male-biased mutation. Proc. R. Soc. B 274, 1–10 (2007).
Kong, A. et al. Fine-scale recombination rate differences between sexes, populations and individuals. Nature 467, 1099–1103 (2010).
Venn, O. et al. Strong male bias drives germline mutation in chimpanzees. Science 344, 1272–1275 (2014).
Cutter, A. D., Jovelin, R. & Dey, A. Molecular hyperdiversity and evolution in very large populations. Mol. Ecol. 22, 2074–2095 (2013). This article discusses the specificities and challenges associated with very highly polymorphic species, with a focus on Caenorhabditis nematodes.
Drouin, G. Characterization of the gene conversions between the multigene family members of the yeast genome. J. Mol. Evol. 55, 14–23 (2002).
Borts, R. H. & Haber, J. E. Meiotic recombination in yeast: alteration by multiple heterozygosities. Science 237, 1459–1465 (1987).
Dobzhansky, T. Evolution, Genetics, and Man (Wiley, 1955).
Ohta, T. Slightly deleterious mutant substitutions in evolution. Nature 246, 96–98 (1973).
Hubby, J. L. & Lewontin, R. C. A molecular approach to the study of genic heterozygosity in natural populations. I. The number of alleles at different loci in Drosophila pseudoobscura. Genetics 54, 577–594 (1966).
Soulé, M. in Molecular Evolution (ed. Ayala, F.) 60–77 (Sinauer Associates, 1976).
Nevo, E., Beiles, A. & Ben-Shlomo, R. in Evolutionary Dynamics of Genetic Diversity: Proceedings of a Symposium held in Manchester, England, March 29–30, 1983 (ed. Mani, G. S.) (Springer, 1984).
Hamrick, J. L. & Godt, M. J. W. Effects of life history traits on genetic diversity in plant species. Phil. Trans. R. Soc. Lond. B 351, 1291–1298 (1996).
Cole, C. T. Genetic variation in rare and common plants. Annu. Rev. Ecol. Evol. Systemat. 34, 213–237 (2003).
Avise, J. C. et al. Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Annu. Rev. Ecol. Systemat. 18, 489–522 (1987).
Bazin, E., Glémin, S. & Galtier, N. Population size does not influence mitochondrial genetic diversity in animals. Science 312, 570–572 (2006).
Nabholz, B., Glémin, S. & Galtier, N. The erratic mitochondrial clock: variations of mutation rate, not population size, affect mtDNA diversity across birds and mammals. BMC Evol. Biol. 9, 1–13 (2009).
Ballard, J. W. O. & Whitlock, M. C. The incomplete natural history of mitochondria. Mol. Ecol. 13, 729–744 (2004).
Berlin, S., Tomaras, D. & Charlesworth, B. Low mitochondrial variability in birds may indicate Hill–Robertson effects on the W chromosome. Heredity 99, 389–396 (2007).
Hurst, G. D. D. & Jiggins, F. M. Problems with mitochondrial DNA as a marker in population, phylogeographic and phylogenetic studies: the effects of inherited symbionts. Proc. R. Soc. B 272, 1525–1534 (2005).
Galtier, N., Nabholz, B., Glémin, S. & Hurst, G. D. D. Mitochondrial DNA as a marker of molecular diversity: a reappraisal. Mol. Ecol. 18, 4541–4550 (2009).
Piganeau, G. & Eyre-Walker, A. Evidence for variation in the effective population size of animal mitochondrial DNA. PLoS ONE 4, e4396 (2009).
Jarne, P. & Lagoda, P. J. L. Microsatellites, from molecules to populations and back. Trends Ecol. Evol. 11, 424–429 (1996).
Väli, Ü., Einarsson, A., Waits, L. & Ellegren, H. To what extent do microsatellite markers reflect genome-wide genetic diversity in natural populations? Mol. Ecol. 17, 3808–3817 (2008).
Fungtammasan, A. et al. Accurate typing of short tandem repeats from genome-wide sequencing data and its applications. Genome Res. 25, 736–749 (2015).
Ellegren, H. Genome sequencing and population genomics in non-model organisms. Trends Ecol. Evol. 29, 51–63 (2014).
Lynch, M. & Conery, J. S. The origins of genome complexity. Science 302, 1401–1404 (2003).
Wright, S. Evolution in Mendelian populations. Genetics 16, 97–159 (1931).
Luikart, G., Ryman, N., Tallmon, D., Schwartz, M. & Allendorf, F. Estimation of census and effective population sizes: the increasing usefulness of DNA-based approaches. Conserv. Genet. 11, 355–373 (2010).
Palstra, F. P. & Fraser, D. J. Effective/census population size ratio estimation: a compendium and appraisal. Ecol. Evol. 2, 2357–2365 (2012).
Gilbert, K. J. & Whitlock, M. C. Evaluating methods for estimating local effective population size with and without migration. Evolution 69, 2154–2166 (2015).
Browning, S. R. & Browning, B. L. Accurate non-parametric estimation of recent effective population size from segments of identity by descent. Am. J. Hum. Genet. 97, 404–418 (2015).
Kirin, M. et al. Genomic runs of homozygosity record population history and consanguinity. PLoS ONE 5, e13996 (2010).
Palamara, P. F., Lencz, T., Darvasi, A. & Pe'er, I. Length distributions of identity by descent reveal fine-scale demographic history. Am. J. Hum. Genet. 91, 809–822 (2012).
Acknowledgements
This work was supported by Swedish Research Council grants (2010–5650 and 2013–8271), a European Research Council grant (AdG 249976) and the Knut and Alice Wallenberg Foundation to H.E., and by a European Research Council grant (AdG 232971) and a French National Research Agency grant (ANR-10-BINF-01-01) to N.G. The authors thank N. Bierne, S. Glemin and M. Lascoux for comments on the manuscript.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Glossary
- Genetic diversity
-
(Also known as genetic polymorphism). Variation in a DNA sequence between distinct individuals (or chromosomes) of a given species (or population).
- Allozymes
-
Allelic variants of proteins that can be separated by electrophoresis based on differences in charge or structure.
- Fixation
-
The complete spread of a mutation in the population such that it replaces all other alleles at a site.
- Genetic drift
-
Fluctuation of allele frequency among generations in a population owing to the randomness of survival and reproduction of individuals, irrespective of selective pressures.
- Effective population size
-
(Ne). The number of breeding individuals in an idealized population that would show the same amount of genetic drift (or inbreeding, or any other variable of interest) as the population under consideration.
- Census population size
-
(Nc).The number of individuals in a population.
- Frequency-dependent selection
-
A form of selection in which the selective advantage or disadvantage of a genotype is dependent on its frequency relative to other genotypes.
- Bottleneck
-
A sharp and rapid reduction in the size of a population.
- Heterozygosity
-
The probability that two randomly sampled gene copies in a population carry distinct alleles; a measure of the genetic diversity.
- Drift-barrier hypothesis
-
The idea, based on the concept of diminishing returns, that selection can only improve a trait up to a point at which the next incremental improvement will be overwhelmed by the power of genetic drift.
- Coalescent theory
-
A retrospective model of the distribution of gene divergence in a genealogy.
- Identity-by-descent segments
-
Chromosomal segments carried by two or more individuals that are identical because they have been inherited from a common ancestor, without recombination.
- Polyploidization
-
A form of genome evolution in which the number of sets of chromosomes increases.
- Linkage disequilibrium
-
The non-random association of alleles at two loci, often but not always due to physical linkage on the same chromosome.
- Selective sweep
-
Elimination or reduction of genetic diversity in the neighbourhood of a beneficial allele that increases in frequency in the population, typically after an environmental change.
- Hard sweeps
-
Selective sweeps in which the beneficial allele corresponds to a single, new mutation appearing after an environmental change.
- Soft sweeps
-
Selective sweeps in which the beneficial allele exists before an environmental change (thus representing standing variation) and is initially neutral or even slightly deleterious, or appears several times independently.
- Genetic draft
-
Pervasive reduction of genetic diversity owing to recurrent selective sweeps.
- Background selection
-
Reduction of genetic diversity owing to selection against deleterious mutations at linked loci.
- Introgression
-
New alleles entering the population by hybridization with members of a differentiated population or even a different species.
- Hitch-hiking
-
The change in allele frequency at a locus that itself is not necessarily affected by selection but is genetically linked to a locus that is.
- Allele frequency spectrum
-
The distribution of the frequency of variants across biallelic loci in a population sample.
- Polygyny
-
A mating system in which males mate with more than one female.
- Polyandry
-
A mating system in which females mate with more than one male.
- Heterogamety
-
When an organism of a particular sex carries two different types of sex chromosomes: that is, males of many animals and plants and females of birds, some fish and lizards, butterflies, and others.
- Hemizygous
-
The situation when there is only one chromosome copy in an individual of a diploid species, as for the X chromosome in males of many species.
Rights and permissions
About this article
Cite this article
Ellegren, H., Galtier, N. Determinants of genetic diversity. Nat Rev Genet 17, 422–433 (2016). https://doi.org/10.1038/nrg.2016.58
Published:
Issue Date:
DOI: https://doi.org/10.1038/nrg.2016.58
This article is cited by
-
Population status and genetic assessment of mugger (Crocodylus palustris) in a tropical regulated river system in North India
Scientific Reports (2024)
-
Population genetics of the endangered Clanwilliam sandfish Labeo seeberi: considerations for conservation management
Aquatic Sciences (2024)
-
Microsatellite and mtDNA-based exploration of inter-generic hybridization and patterns of genetic diversity in major carps of Punjab, Pakistan
Aquaculture International (2024)
-
Employing plant DNA barcodes for pomegranate species identification in Al-Baha Region, Saudi Arabia
Journal of Umm Al-Qura University for Applied Sciences (2024)
-
Metabolomic profiling of wild rooibos (Aspalathus linearis) ecotypes and their antioxidant-derived phytopharmaceutical potential
Metabolomics (2024)